PHYLUM FORAMINIFERA – Diversity of Life

EUKARYA> CHROMALVEOLATA> RHIZARIAE> FORAMINIFERA

Foraminifera (fore-am-in-IFF-ur-uh) is derived from two Latin roots roots that mean an opening (foramen) and to bear (ferre). The reference is to a test that covered with pores. Thus, the forams are the pore-bearers.

INTRODUCTION TO THE FORAMINIFERA

The Foraminifera, informally called forams, generally are members of the marine plankton and benthos where they can be very abundant and diverse. They capture their food by filtering the surrounding water with a reticulate , anastomosing pseudopodial web. There are four general types of forams: athalamids, monothalamids, polythalamids, and xenophyophorids. These groupings are of descriptive, rather than taxonomic value.

Athalamids have no test and, therefore, resemble the filose amoebae of the Endomyxa and Cercozoa. Reticulomyxa (Figure 1), first recognized as a freshwater foram by Pawlowski et al. (1999), is quite large, and in form, may help us understand what the earliest forms looked like and how they lived. Though forams have an almost continuous fossil record from the lower Cambrian, Groussin et al. (2011), in a molecular analysis of forams whose molecular clock was calibrated by foram fossils, suggest that they likely appeared during the Neoproterozoic (between 650 and 920 million years ago). Thus, naked forams, or cells with tests that are not mineralized, may have occurred for 150 to nearly 400 million years before mineralized tests appeared.

Allogromia (Figure 2) is an monothalamid (cells with tests having a single chamber) with an organic test, also a form that is unlikely to leave a fossil record. These are marine are marine taxa with somewhat elaborate life histories (see Figure 3). They have an alternation of generation that includes a uninucleate haploid gamont and a multinucleate diploid agamont. The gamont undergoes multiple mitotic divisions within the gamont test. The hundreds of resulting cells develop into heterodynamic motile isogametes that fuse to produce a zygote, which develops into a multinucleate agamont. Meiosis occurs within the agamont, which releases haploid, nonmotile spores that develop into gamonts.


FIGURE 1. A photomicrograph of Reticulomyxa, a naked freshwater foram. Note the extensive field of reticulopods surrounding the elongate the cell. Image from The Molecular Systematics Group	FIGURE 2. Allogromia has a proteinaceous test with a single chamber. Image from: http://www.unige.ch/sciences/biologie/biani/msg/people/Fabien/Gromia2.htm

FIGURE 3. Life History of Myxotheca.

1. Haploid gamont
2. Gametogenesis
3. Syngamy of isogametes
4. Zygote
5. Developing diploid agamont
6. Mature diploid agamont
7. Meiosis of agamont nuclei
8. Sporogenesis
9. Developing haploid spore to form a gamont

Image from Grell (1973).

Most of the remaining groups of forams make an internal test of calcium carbonate that may or may not be perforated by patterns of holes. Often, the tests are quite complex with multiple chambers that increase in size, somewhat reminiscent of a Nautilus shell [e.g. Globigerina (Figure 4), Textularia (Figure 5)]. They have a decided and complex alternation of generation and dimorphic nuclei like the ciliates. Consider the life history of a complex foram like Metarotaliella (see Figure 4). The gamont (1 in Figure 4) is haploid and associates with one or more other gamonts. They hold themselves in place by secreting a copulation jelly and then the gamonts undergo multiple mitoses with cytokineses to form many gametes. Compatible mating types fuse to form zygotes. The diploid cells begin to undergo mitosis without cytokinesis forming multinucleate cells. After they reach 4 nuclei, one enlarges and becomes polyploid to become the somatic nucleus (analogous to the macronucleus of a ciliate). As the cell enlarges, more calcareous chambers are added until finally the somatic cells undergo meiosis and the somatic nucleus aborts and is reabsorbed. The resulting 12 haploid nuclei accrete cytoplasm and become 1-chambered gamonts that begin to enlarge until copulation is triggered. Only through this complex alternation of generation can they increase numbers of cells.

The complex polythalamid type of cell and life history seems to have been quite successful. From the appearance of mineralized taxa (e.g. Figure 4) and those with mixture of mineral and attached sediment grains (Figure 5) in the fossil record during the Cambrian, they have persisted to the present in great abundance and diversity. They are so common in marine sediments that forams to be among the most useful index fossils for marine strata. For that reason also they are among the most useful index fossils to use in oil exploration.

Nummulites is a very large (up to 6 cm in diameter) foram from the early Tertiary (Eocene). It looked like Figure 7, and its name in Latin means little coin. They were so abundant in the shallow seas that covered part of Egypt, that their accumulated tests were major components of the thick beds of limestone from which the outer sheathing stones of the great pyramids were made.

Xenophylophorids are huge amoeboid cells that likely are benthic forams that have barium sulfate crystals in their spongy tests (Figure 8). Some can be as large as 24 cm across (but very thin). There is little unanimity on their relationships, and the xenophyloporids may have to move to another kingdom.


FIGURE 4. Globigerina makes a wall of hyaline calcite with many regularly-arranged perforations. This genus is found in almost all latitudes from the tropics to the subpolar seas. Image from: http://www.ucmp.berkeley.edu/people/klf/MicroGalleryLarge_files/Globigerina.jpg	FIGURE 5. Textularia has a test made of two off-set series of chambers that are partly mineralized and covered with sand grains. Image from: http://coastal.er.usgs.gov/biscayne-forams/gallery.html	FIGURE 7. Photomicrograph of a split test of Nummulites, an Eocene fossil. Note the multiple chambers in the test. Image from the Systematic Biology Biodiversity Archive	FIGURE 8. Cerelpemma, a xenophyophorid produces a lumpy irregular test that is sponge-like in its form. From 4-6 km deep in the Pacific Ocean. Image from Gooday and Tendal (2000)

FIGURE 6. Life History Metarotaliella.

1. Gamont
2. Mating of 2 gamonts
3. Gametes in the parent tests that are held together by copulation jelly
4. Zygotes
5. Binucleate agamonts
6. Agamonts with 4 undifferentiated nuclei
7. Agamonts with 4 nuclei (3 are generative and one is somatic)
8. Mature agamont
9. Meiosis of generative nuclei
10. Second meiotic division
11-12. Haploid nuclei and differentiation to spores, each of which will develop into a gamont.

Image from Grell (1973).

SYSTEMATICS OF THE FORAMINIFERA

As it is defined here, the descriptions of the Foraminifera are from Lee (1990) and of Margulis and Schwartz (1988 and 1998) in which it is designated Pr-17 and PR-4, respectively. Kudo (1966), Grell (1976), Cushman (1980), Bovee (1985b), Bock et al. (1985) and Sleigh et al. (1984) lump the forams together with the amoebae, the slime molds and the actinopods. Forams are clearly different from the other “amoeboid” groups. The reticulopods produced by the forams are neither pseudopods nor actinopods (Margulis and Schwartz 1988 and 1998). Patterson (1989) suggests a connection with the chrysophyte complex based on the flagella produced by their motile cells (a view that he later -1999- repented of). Patterson (1999) gives the web-branching pseudopodial system as a possible synapomorphy for the group. The Xylophylophorids have been taxonomic nomads for a long time, but from the time of their discovery they have been referred to as benthic forams (Tendal 1972; Patterson 1999). Thus, we have kept the xenophyophorids together with the forams, but in their own class despite the misgivings of Lee et al. (2000).

All Foraminifera have granular cytoplasm, a trait that they have in common with some other rhizarian amoebae. That character was once considered to be the defining feature of a broader phylum called Granuloreticulosa (e.g. Lee et al. 2000), in which the Foraminifera were just one group. The elimination of problematic taxa (formerly in the Athalamea, a formal taxon that has been abandoned) like Gromia has simplified the systematics of the group. Those taxa that have been examined all have a single polyubiquitin insertion (Bass et al. 2005).

Longet et al. (2003), Archibald et al. (2003), Archibald and Keeling (2004), and Nikolaev et al. (2004) show clear relationships between the foraminifera and taxa that are in the emerging supergroup called Cercozoa (or Rhizaria after Cavalier-Smith 2002). Baldauf (2003) and Keeling (2004) produced a synthesis of molecular and structural analyses that suggested the eukaryotes occupy eight (or five) major clades. The diversity of form, complexity of life history, and the occurrence of dimorphic nuclei all argue for raising the Foraminifera to phylum-level rank. The class-level ranks of forams and the relationships with the Radiolaria, in a group that Cavalier-Smith (1999) called Retaria, has been recovered in molecular analyses that examine a broad sample of relevant taxa (e.g. Nikolaev et al 2004, Ishitani et al. 2011).

The relationships between groups of forams monothalamids, and multiple groups of polythalamids are problematic (Pawlowski and Holzmann 2002, Groussin et al. 2011, Longet and Pawlowski 2007). Consistently, the monothalamids form a paraphyletic basal group of taxa. Furthermore, it does appear that the xenophyophorids do emerge from within the polythalamids (Pawlowski et al. 2003). If so, there is a single class. So, because of inadequate taxonomic sampling, the systematics of the forams remains messy. At present, we fall back on a modification of the system of Lee (2000) until a complete system is erected. This has two classes (shown as sisters in Figure 9).

FIGURE 9. A cladogram based on Pawlowski et al. (2003) and Groussin et al. (2011) showing a simplified view of the relationships between the two major taxa of the Foraminifera (those taxa highlighted in the shaded box).

LITERATURE CITED

Adl, S. M., A. G. B. Simpson, M. A. Farmer, R. A. Andersen, O. R. Anderson, J. R. Barta, S. S. Bowser, G. Brugerolle, R. A. Fensome, S. Fredericq, T. Y. James, S. Karpov, P. Kugrens, J. Krug, C. E. Lane, L. A. Lewis, J. Lodge, D. H. Lynn, D. G. Mann, R. M. McCourt, L. Mendoza, O. Moestrup, S. E. Mozley-Standridge, T. A. Nerad, C. A. Shearer, A. V. Smirnov, F. W. Spiegel, and M. F. J. R. Taylor. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. Journal of Eukaryotic Microbiology. 52(5):399-451.

Archibald, J. M. and P. J. Keeling. 2004a. Actin and ubiquitin protein sequences support a cercozoan/foraminiferan ancestry for the plasmodiophorid plant pathogens. Journal of Eukaryotic Microbiology. 51(1):113-118.

Archibald, J. M., D. Longet, J. Palowski, and P. J. Keeling. 2003. A novel plolyubiquitin structure in Cercozoa and Foraminifera: Evidence for a new eukaryotic supergroup. Molecular Biology and Evolution. 20:62-66.

Baldauf, S. L. 2003. The deep roots of eukaryotes. Science. 300(5626): 1701-1703.

Bass, D., D. Moreira, P. Lopez-Garcia, S. Polet, E. E. Chao, S. von der Heyden, J. Pawlowski, and T. Cavalier-Smith. 2005. Polyubiquitin insertions and the phylogeny of Cercozoa and Rhizaria. Protist. 156: 149-161.

Bass, D., E. E.-Y. Chao, S. Nikolaev, A. Yabuki, K. Ishida, C. Berney, U. Pakzad, C. Wylezich, and T. Cavalier-Smith. 2009. Phylogeny of novel naked filose and reticulose Cercozoa: Granofilosea cl. n. and Proteomyxidea revised. Protist. 160: 75-109.

Beech, P. L. and Ø. Moestrup. 1986 Light and electron microscopical observations on the heterotrophic protist Thaumatomastix salina comb. nov. (syn. Chrysosphaerella salina) and its allies. Nordic Journal of Botany. 6(6): 865 – 877.

Bock, W., W. Hay and J. J. Lee. 1985. Order Foraminiferida. In: Lee, J. J., S. H. Hunter, and E. C. Bovee, eds. An Illustrated Guide to the Protozoa. Allen Press. Lawrence, Kansas. pp. 252-273.

Bovee, E.C. 1985b. Order Athalamida; Order Monothalamida. In: Lee, J. J., S.H. Hunter, and E.C. Bovee, eds. An Illustrated Guide to the Protozoa. Allen Press. Lawrence, Kansas. pp. 246-252.

Cavalier-Smith, T. 2002a. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. International Journal of Systematic Evolutionary Microbiology. 52:297–354.

Cavalier-Smith, T. 2003a. Protist phylogeny and the high-level classification of Protozoa. European Journal of Protistology. 39:338-348.

Cavalier-Smith, T. and E. E. Chao. 2003a. Phylogeny and classification of phylum Cercozoa (Protozoa). Protist. 154: 341-358.

Cushman, J.A. 1980. Foraminifera; their classification and economic use. 4th Edition. Harvard University Press. Cambridge, Mass.

Febvre-Chevalier, C. 1990. Heliozoa. In: Margulis, L., J. O. Corliss, M. Melkonian, and D. J. Chapman, eds. 1990. Handbook of the Protoctista; the structure, cultivation, habits and life histories of the eukaryotic microorganisms and their descendants exclusive of animals, plants and fungi. Jones and Bartlett Publishers. Boston. pp. 347-362.

Grell, K. G. 1973. Protozoology. Springer-Verlag. New York.

Keeling P. J. 2004 The diversity and evolutionary history of plastids and their hosts. American Journal of Botany. 91(10): 1481-1493.

Kudo, R.R. 1966. Protozoology. 5th ed. Charles C. Thomas Publisher. Springfield.

Kuhn, S., M. Lange, and L. K. Medlin. 2000. Phylogenetic position of Cryothecomonas inferred from nuclear-encoded small subunit ribosomal RNA. Protist. 151: 337-345.

Lee, R. E. 1999, Phycology: 3rd ed., Cambridge University Press, Cambridge, UK.

Lee, J. J. 1990. Phylum Granuloreticulosa (Foraminifera). In: Margulis, L., J. O. Corliss, M. Melkonian, D. J. Chapman, and H. McKhann. Handbook of Protochtista, the structure, cultivation, habits, and life histories of the eukaryotic microorganisms and their descendants exclusive of animals, plants, and fungi. Jones and Bartlett Publishers. Boston. pp. 524-548 [L]

Lee, J. J., S. H. Hunter, and E. C. Bovee, eds. 1985. An Illustrated Guide to the Protozoa. Society of Protozoologists. Lawrence, Kansas.

Lee, J. J., J. Pawlowski, J.-P. Debenay, J. Whittaker, F. Banner, A. J. Gooday, O. Tendal, J. Haynes, and W. W. Faber. 2000. Phylum Granuloreticulosa. In: Lee, J.J., G.F. Leedale, and P. Bradbury. An Illustrated Guide to the Protozoa. 2nd edition. Society of Protozoologists.Lawrence KS. (Year 2000). pp.872-951.

Longet, D., J. M. Archibald, P. J. Keeling, and J. Pawlowski. 2003. Foraminifera and Cercozoa share a common origin according to RNA polymerase II phylogenies. International Journal of Systematic and Evolutionary Microbiology. 53: 1735-1739.

Margulis, L. and K. Schwartz. 1988. Five kingdoms, an illustrated guide to the phyla of life on earth. 2nd Edition. W.H. Freeman and Co. New York.

Margulis, L. and K. Schwartz. 1998. Five kingdoms, an illustrated guide to the phyla of life on earth. 3rd Edition. W. H. Freeman and Company. New York.

Nikolaev, S. I., C. Berney, J. Fahrni, I. Bolivar, S. Polet, A. P. Mylnikov, V. V. Aleshin, N. B. Petrov, and J. Pawlowski. 2004. The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proceedings of the National Academy of Sciences. USA. 101(21): 8066-8071.

Patterson, D. J. 1989. Stramenopiles: chromophytes from a protistan perspective. In: Green, J.C., B.S.C. Leadbeater, and W.L. Diver, eds. The chromophyte algae, problems and perspectives. Systematics Association Special Volume No. 38. Clarendon Press. Oxford. pp. 357-379.

Patterson, D. J. 1999. The diversity of eukaryotes. American Naturalist. 154 (Suppl.): S96–S124.

Patterson, D. J. and M. Zölffel. 1991. Heterotrophic flagellates of uncertain taxonomic position. In: Patterson, D. J. and J. Larsen, eds. The Biology of Free-Living heterotrophic Flagellates. Clarendon Press. Oxford. pp. 427-475.

Pawlowski, J., I. Bolivar, J. Fahrni, C. de Vargas, S. S. Bowser. 1999. Molecular evidence that Reticulomyxa filosa is a freshwater naked foraminifer. Journal of Eukaryotic Microbiology. 46(6): 612-617.

Pawlowski, J., I. Bolivar, J. Fahrni, C. de Vargas, S. S. Bowser. 1999. Naked foraminiferans revealed. Nature 399: 27.

Pawlowski, J. 2000. Introduction to the molecular systematics of Foraminifera. Micropaleontolgy. 46: 1-12.

Pawlowski, J., M. Holzmann, C. Berney, J. Fahrni, T. Cedhagen, A. Habura, and S.S. Bowser. 2002. Phylogeny of allogromiid Foraminifera inferred from SSU rRNA gene sequences. J. Foram. Res. 32:334-343.

Pawlowski, J., M. Holzmann, J. Fahrni, and S. L. Richardson. 2003. Small subunit ribosomal DNA suggests that the Xenophorean Syringammina corbicula is a foraminiferan. Journal of Eukaryotic Microbiology. 50:483-487.

Pawlowski, J. 2008. The twilight of Sarcodina: a molecular perspective of the polyphyletic origin of amoeboid protists. Protistology. 5(4): 281-302.

Pawlowski, J. and F. Burki. 2009. Untangling the phylogeny of amoeboid protists. Journal of Eukaryote Microbiology. 56(1): 16-25.

Sleigh, M. A., J. D. Dodge and D. J. Patterson. 1984. Kingdom Protista. In: Barnes, R.K.S., ed. A Synoptic Classification of Living Organisms. Sinauer Associates, Inc. Sunderland, Mass.

Tendal, O. S. 1972. A Monograph of the Xenophyophoria (Rhizopodea, Protozoa). Galathea Report. 12: 7-99.

By Jack R. Holt. Last revised: 03/06/2013

PHYLUM FORAMINIFERA (d’Orbigny 1826)

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